Trust-Threat “Positivity” Bias

In document Real World Social Cognition: Context Effects in Face and Threat Processing (Page 65-130)

Separate examination of an approach-related “positivity” bias (positive for faces with stronger trust than threat ratings) for whole and occluded faces separately revealed a default positive approach bias to occluded but not whole faces in both controls and patients (Figure 2.2.7). While a shift between whole positivity ratings (M=0.063) and occluded positivity ratings (M=0.656) was present in controls (p=5.90x10-10), this shift in positivity bias for occluded faces was markedly greater in the patients (M =0.373 for whole vs. M =1.618 for occluded faces, p=0.0199).

Figure 2.2.7. Bootstrap comparison of patients and controls approach-related “positivity” biases. Density plot estimates of three randomly sampled controls’ mean positivity bias

-2 -1 0 1 2 3 0 0.2 0.4 0.6 0.8 1

Trust-Threat “Positivity” Bias

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Patients Occluded 4.2% 28.3%

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(black lines), and the actual patients’ mean positivity bias (blue lines) for whole (solid lines) and occluded (dashed lines) faces. Patients and controls both had a greater approach- related positivity bias for occluded than whole faces, but the magnitude of the shift was greater for the patients, who were also most distinct from controls for the occluded faces specifically. *p<0.05; ***p<0.001.

Results Separated by Judgment and Stimulus Type

Across comparisons, an occluded approach bias was defined as a tendency to give both higher trust (“Yes,” trustworthy) and lower threat (“No,” not threatening) ratings to occluded faces than to whole faces. While a composite approach bias was the most comprehensive way to describe our results, separate trust and threat biases obviously contribute to this construct. We thus also compared the lesion patients’ mean trust and threat occluded biases separately to bootstrapped control distributions, alongside patient performance for whole and occluded faces alone (Table 2.2.2), confirming that the patients’ observed approach bias was driven by abnormal ratings of occluded faces.

Table 2.2.2. Bootstrapped control samples exceeding mean and individual patient values.

Judgment Stimuli Controls

Exceeding Patients (%) Control Mean (95% CI) AP AM BG Summary

Threat Whole faces 19.9 [3.2, 3.4] 3.3 2.7 3.2 AP & BG same, but AM lower

Occluded faces 4.7 [2.8, 3.1] 2.6 2.2 2.1 All lower

Occluded bias 12.1 [-0.5, -0.3] -0.7 -0.4 -1.1 AP and BG lower; AM not different,

but already impaired for whole faces

Trust Whole faces 23.7 [3.1, 3.3] 3.1 2.6 4.6 AP normal; AM low; BG high

Occluded faces 3.9 [3.3, 3.5] 3.3 3.4 5.0 AP and AM normal; BG very high

Occluded bias 8.9 [0.1, 0.3] 0.2 0.8 0.4 AP normal; AM and BG high

Composite Bias

All faces 7.6 [0.4, 0.8] 0.9 1.2 1.6 All higher

Occluded- avoided faces

1.9 [-0.8, -0.4] 0.2 0.4 1.2 All higher

Occluded- approached faces

15.8 [0.8, 1.2] 1.2 1.5 1.7 AP normal; AM and BG higher

Note. Occluded bias defined as occluded minus whole face rating. Composite bias defined as occluded trust bias minus occluded threat bias. Occluded-avoided faces have a negative average composite bias score; occluded-approached faces have a positive average composite bias score. For threat, the percentage of lower bias scores were counted; for trust and composite bias, the percentage of higher scores were counted.

As a group, the patients’ whole-face ratings were not different from controls’ ratings, which was somewhat unexpected given a previous finding in amygdala lesion patient SM (Adolphs et al., 1998), which showed that SM gave abnormally high trustworthiness judgments to whole faces (albeit a different set of faces than the ones used in our present

study). To verify that this discrepancy from SM’s behavior in our amygdala lesion patients was not driven by differences in the stimulus sets, we tested two of our patients (AM and BG) also on the original stimuli from that experiment with SM (Adolphs et al., 1998). While AM and BG tended to deviate from controls, especially for the faces controls avoided most (Figure 2.2.8), they only exhibited a weak trend towards the prior finding in SM. Unfortunately, SM was not available for testing in our new task, and AP was not available for testing on the original task used by Adolphs et al. (1998).

Figure 2.2.8. Amygdala lesion patients’ deviations from normal judgments of

approachability (top) and trustworthiness (bottom) of 100 faces (circles; y-axis). Units are standard deviations of the normal control ratings. Stimuli are rank-ordered on the x-axis according to the ratings normal controls gave them. SM demonstrated a specific exaggerated impairment in her ratings of the faces rated least approachable or trustworthy

all faces. SM’s panels recreated with data from Figure 2 of Adolphs, Tranel, and

Damasio, Nature, 1998.

Discussion

A significantly enhanced approach-related bias, relative to controls, was uncovered in three rare patients with selective bilateral amygdala lesions by comparing ratings of faces in a whole and occluded condition. A default bias was demonstrated by the patients’ greater willingness to approach a face (i.e., less threatening and more trustworthy ratings) in the low-information occluded condition.

Returning to our example situation of walking into a dark room, the normal response to an ambiguous situation is risk-assessment (Blanchard et al., 2011) — given insufficient information to determine whether a threat is present, one should pause and gather more information before proceeding; our patients’ ratings indicated that they would simply enter the room; at the other end of the spectrum, anxious individuals might flee the dark room before gathering further evidence. Future experiments exploring individual differences (e.g., trait/state anxiety, perceived dominance, history of exposure to physical/social threat or betrayal) will be important to both validate our task and determine what factors beyond amygdala damage relate to heightened approach tendencies. It is worth noting that in our sample a few control individuals had an approach bias similar to that of the patients, emphasizing the importance of future studies to determine the cause of these individual differences.

In humans, given a lack of stimulus information, an exploratory tendency may normally promote a default approach bias, the “positivity offset” in the Evaluative Space Model (Norris et al., 2010), similar to our observed shift in “positivity” approach ratings

between the occluded and whole face conditions (Figure 2.2.7). This occluded positivity bias was observed both in controls and patients, but enhanced in the patients. It is worth noting that while in this class of stimuli a lack of information, which was similar to

ambiguity, encouraged approach behavior in both healthy controls and the amygdala lesion patients, for some classes of stimuli, given some additional contextual cues, ambiguity in and of itself might be perceived as threatening and prompt avoidance behavior, especially in healthy controls.

While patients gave stronger approach ratings than controls, they were not

completely indiscriminate: their judgments differed more in degree than direction (Table 2.2.2). Future work should test how their enhanced approach bias extends to (1) other classes of degraded stimuli (including non-linguistic tasks to better facilitate cross-cultural comparison), and (2) the real world. Showing abnormal proxemic (i.e, personal space) behavior and a tendency to approach real threatening stimuli (e.g., snakes) in these three patients, as has already been done in patient SM (Feinstein et al., 2011; Kennedy et al., 2009), would further corroborate a default approach bias. As confirmed in preliminary testing, at least BG has abnormally small personal space and fear responses (D.P. Kennedy, J. Feinstein, & R. Adolphs, personal communication). Testing participants’ actual behavior is crucial – compensatory processing may allow them to give more “correct” explicit ratings: for example, although SM abnormally approached actual snakes without showing any fear, beforehand, she verbally insisted that she “hates” snakes and “tries to avoid them” (Feinstein et al., 2011).

Differences amongst the amygdala lesion patients need to be resolved. Amygdala damage can prompt two distinct approach processes — a default bias, as well as a face-

specific bias — both of which can operate simultaneously. Removing facial feature information from facial stimuli allowed us to challenge participants to indicate a default bias while working within the general category of facial stimuli. Across all participants, responses to facial features were variable and the patients were similar to controls. SM’s whole face ratings had been different from controls (Adolphs, et al., 1998); this deviation is in line with the heterogeneity of impairments reported in bilateral amygdala damage

(Adolphs et al., 1999; Hamann et al., 1996; Siebert, Markowitsch, & Bartel, 2003) and likely reflects compensatory processing (Becker et al., 2012; Scheele et al., 2012). SM’s impairment for whole faces hints at progressive amygdala damage/impairment, as is expected in Urbach-Wiethe disease (Appenzeller et al., 2006).

While patient differences in a face specific deficit need to be further explored and explained based on precise anatomical differences, the present study focused on isolating a stimulus-independent shift, which will clearly interact with responses to facial features. Sometimes, “good” facial features (determined idiosyncratically) helped occluded-avoided faces; sometimes “bad” features harmed occluded-approached faces. However, across the entire stimulus set, a general occluded-approach bias could be observed.

Mechanistically, the patients’ approach bias may relate to a specific cautionary deficit, related to disrupted vigilance (Davis & Whalen, 2001; Paul J. Whalen, 2007). This viewpoint is anatomically compatible with the amygdala launching a defensive behavioral response to coincident sensory and contextual danger signals, conveyed via the temporal and prefrontal cortices, respectively (Freese & Amaral, 2009).

However, the patients’ approach bias can be explained by a more general mechanism of amygdala function. A general role in processing saliency/self-relevance (Cunningham

& Brosch, 2012; Harrison & Adolphs, 2015; Sander, Grafman, & Zalla, 2003) is

compatible with a wider array of known amygdala activity. The amygdala contributes to negative and positive reinforcement (Murray, Izquierdo, & Malkova, 2009), and processes positively and negatively valenced stimuli (Anderson et al., 2003; Hamann et al., 2002). In rats (Hatfield, Han, Conley, Gallagher, & Holland, 1996) and nonhuman primates

(Izquierdo & Murray, 2007; Málková, Gaffan, & Murray, 1997), basolateral amygdala lesions interfere with reinforcer devaluation, such that an animal will indiscriminately approach devalued food items, similar to our patients’ default approach bias.

Hypothetically, the basolateral nucleus, damaged in our patients, updates the self-relevant value of a stimulus (Murray et al., 2009).

A saliency/relevance explanation binds our default bias finding with prior findings in amygdala lesion patients: amygdala lesions do not preclude the ability to experience fear - indeed, CO2 inhalation can induce fear and panic in amygdala lesion patients (Feinstein et

al., 2013), but instead inhibit proper orienting to stimuli (Spezio, Huang, Castelli, & Adolphs, 2007), which often results in a diminished ability to experience (Feinstein et al., 2011) or recognize (Adolphs et al., 2005) fear. Proper orienting can recover this ability: in SM, fear is correctly identified following explicit top-down instruction to look at the eyes (Adolphs et al., 2005).

Our finding of an enhanced default positivity bias suggests a further role for the amygdala in setting a default on what is potentially relevant or salient, normally preventing us from approaching situations that may be threatening, while simultaneously permitting exploration. In our patients, this balance is shifted. Similarly, in psychiatric disorders featuring dis-regulation of the amygdala (e.g., anxiety disorders (Davis, 1992; Etkin &

Wager, 2007) and autism (Baron-Cohen et al., 2000; Castelli, Frith, Happe, & Frith, 2002; Dalton et al., 2005)), stimuli are not correctly evaluated, from shifted baseline biases as well as under- or over-weighting the threat, social importance, or relevance of stimuli.

In summary, contrasting judgments of occluded and whole faces, we uncovered a stimulus-independent approach bias following bilateral amygdala damage. Future directions include (1) testing for a default approach or avoidance bias in

psychiatric disorders for which the amygdala is implicated, as well as (2) developing implicit tests of an approach bias to circumvent potential compensatory mechanisms, and (3) devising tests to provide a clearer mechanistic account of our findings.

C h a p t e r 2 . 3

ECOLOGICAL STRUCTURING OF HUMAN DEFENSIVE RESPONSES: EVIDENCE FROM JUDGMENTS OF PHYSICAL AND PSYCHOLOGICAL THREAT SCENARIOS How humans react to threats is a topic of broad theoretical importance, and also relevant for understanding anxiety disorders. Many animal threat reactions exhibit a common structure, a finding supported by human evaluations of written threat scenarios that parallel patterns of rodent defensive behavior to actual threats. Yet the factors that underlie these shared behavioral patterns remain unclear. Dimensional accounts rooted in Darwin’s conception of antithesis explain many defensive behaviors. Across species, it is also clear that defensive reactions depend on specific situational factors, a feature long emphasized by psychological appraisal theories. Our study sought to extend prior

investigations of human judgments of threat to a broader set of threats, including natural disasters, threats from animals, and psychological (as opposed to physical) threats. Our goal was to test whether dimensional and specific patterns of threat evaluation replicate across different threat classes. 85 healthy adult participants selected descriptions of defensive behaviors that indicated how they would react to 29 threatening scenarios. Scenarios differed with respect to ten factors, e.g., perceived dangerousness or escapability. Across scenarios, we correlated these factor ratings with the pattern of defensive behaviors endorsed. A decision tree hierarchically organized these correlation patterns to successfully predict each scenario’s most common reaction, both for the original sample and a separate replication group (n=22). At the top of the decision tree, degree of dangerousness interacted with threat type (physical or psychological) to

predict dimensional approach/avoidance behavior. Subordinate nodes represented specific defensive responses evoked by particular contexts. Our ecological approach emphasizes the interplay of situational factors in evoking a broad range of threat reactions. Future studies could test predictions made by our results to help understand pathological threat processing, such as seen in anxiety disorders, and could begin to test underlying neural mechanisms.

Introduction

Darwin famously noted the striking phylogenetic continuity of emotional behaviors, including responses to threat (Darwin, 1872/1965). Defensive behaviors, ranging from flight to attack, have evolved to deal with environmental challenges that show a common structure across all animals: the need to attack an aggressor, to flee a predator, or to hide from an inescapable threat, to name only a few prototypical situations. Over the years, several empirical and theoretical studies, largely rooted in biology and ethology, have supported the idea of common structure in defensive behaviors across species, ranging from rodents to humans (Blanchard, Hynd, Minke, Minemoto, & Blanchard, 2001). Various schemes have been proposed for how these are organized, ranging from ethologically-identified (Blanchard, Blanchard, & Hori, 1989) factors like risk assessment (Blanchard et al., 2011) to dimensional accounts including threat imminence (Fanselow & Lester, 1988) and a classic approach/avoidance account whereby all motivated/emotional behaviors are organized along an appetitive and defensive system (Lang, Bradley, & Cuthbert, 1998).

On the other hand, the literature in affective psychology has rarely incorporated specific details of the data from nonhuman animals, although this literature clearly does

acknowledge the biological roots of human defensive behaviors (Lazarus, 1991;

McNaughton & Corr, 2004, 2009; Adam M. Perkins, Cooper, Abdelall, Smillie, & Corr, 2010). Here, we asked people to select hypothetical defensive behaviors to descriptions of a range of physically threatening situations, as well as to situations of social

psychological threat. It is important to emphasize at the outset that we rely on verbal report and ratings, as is common in many psychological studies in humans (e.g., (Cottrell & Neuberg, 2005)), rather than on actual observed defensive behavior. Verbal report to hypothetical scenarios by humans has been found in previous studies to correlate with actual rodent behavior patterns across three laboratories (Blanchard et al., 2011), and we used it here as a first approach to assess responses for which live exposure would be ethically difficult to obtain. Specifically, in the current experiment, threatening situations include situations of social psychological threat, (e.g., blackmail), social physical threat (e.g., stalking), as well as physical threat from other species and natural disasters. Inclusion of these different threat categories underlies an attempt to bridge our understanding of basic approach-avoidance reactions to predators and other physical threats on the one hand, with a characterization of defensive reactions to less physical but more psychological intra-species threats that relate to issues of social inclusion, social hierarchies, and social dominance on the other hand. It is worth noting that socially modulated threat reactions have been observed across diverse phylogenetic classes, including fish (Fernald, 2012), and mammals (Tamashiro, Nguyen, & Sakai, 2005) ranging from rodents (Scheibler, Weinandy, & Gattermann, 2004) to primates (Abbott et al., 2003; Dewaal, 1986).

Defensive behaviors in rodents and primates have been extensively

studied, and related to human behavior, such as in the case of humans physically freezing in response to threatening stimuli (Hagenaars, Oitzl, & Roelofs, 2014). Innate patterns of defensive behavior have been identified in some detail in rats: e.g., high magnitude threats elicit a flight response, only if an escape route is available; if an escape route is not available, rodents will freeze, show a defensive threat (e.g., vocalization), or launch an explosive defensive attack depending on the distance of the threat (Blanchard & Blanchard, 1989). Very specific releasing-stimulus like cues can be sufficient to trigger the behavior: for instance, a predator-like visual looming stimulus (just an expanding black circle on the ceiling) is sufficient to produce robust freeze or flight (Yilmaz & Meister, 2013), with the likelihood of each behavior dependent upon the presence of a hiding place in the arena. The size of an enclosure also seems to affect the use of flight or freeze behavior (Kim et al., 2013). The validity of the use of rodent defensive behaviors as a model for human defensive reactions remains an open question, partially addressed by a study that attempted to make direct comparisons between the two species (Blanchard et al., 2001). In that study, written descriptions of physically threatening scenarios were manipulated in terms of factors known to alter rodent behavior, such as the magnitude of threat, escapability of the situation, ambiguity of the threat stimulus, distance between the threat and the subject, and the presence of a hiding place. Strikingly, most of the human participants’ choices of what they would do when faced with these scenarios paralleled the rodent behavior observed when a rat faced the same real situational factors.

Moreover, the human choices of defensive behaviors paralleled the specific animal defensive behaviors (e.g., defensive attack for near threats; risk assessment for

ambiguous threats; hiding when there is a hiding place) across different cultural settings (see Table 2.3.6, Discussion), e.g., in Brazil (Shuhama, Del-Ben, Loureiro, & Graeff, 2008)and Wales(Perkins & Corr, 2006)with “minor or potentially easily explained differences” (Blanchard et al., 2011) compared to the original patterns observed in Hawaiian participants (Blanchard et al., 2001), suggesting cross-cultural generality at least for the physically threatening scenarios investigated in those studies.

These prior studies that built upon rodent behaviors fit well with

dimensional accounts of emotion. Although Darwin is often cited in support of discrete emotion theories, Darwin’s early principle of antithesis (Darwin, 1872/1965) in fact set the framework for conceiving of emotional behaviors as having a dimensional structure:

When actions of one kind have become firmly associated with any sensation or emotion, it appears natural that actions of a directly opposite kind…should be unconsciously performed…under the influence of a directly opposite sensation or emotion. (p. 67)

Darwin’s notion of antithesis roughly maps onto the modern dimension of “valence”. However, the main point that he made, of course, was that emotions, including defensive behaviors, in humans would look similar and have a similar structure to that of other mammals. According to one theory, evolutionary selection can give rise to what have been called “rules of thumb” that advantageously guide behavior under typical ecological conditions (McNaughton & Corr, 2009). These rules of thumb can be conserved across species that have evolved in similar environments, such that emotional behaviors evoked by certain circumstances in one species will evoke similar emotional behaviors in another

In document Real World Social Cognition: Context Effects in Face and Threat Processing (Page 65-130)